Early postnatal genistein administration permanently affects nitrergic and vasopressinergic systems in a sex-specific way

Neuroscience

Volumn 346, Issue , 2017, Pages 203-215

  Ponti, G ^a   Rodriguez Gomez, A ^a   Farinetti, A ^a   Marraudino, M ^a   Filice, F ^a,b   Foglio, B ^a   Sciacca, G ^a   Panzica, G C ^a   Gotti, S ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

endocrine disruptors; hypothalamus; limbic system; phytoestrogens; sexual dimorphism

Indexed keywords

ESTRADIOL; GENISTEIN; NITRIC OXIDE SYNTHASE; OIL; VASOPRESSIN; NEURONAL NITRIC OXIDE SYNTHASE; PHYTOESTROGEN; VASOPRESSIN DERIVATIVE;

ADULT; AMYGDALA; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONNECTOME; CONTROLLED STUDY; FEMALE; HABITUATION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NITRERGIC NERVE CELL; NONHUMAN; PERINATAL PERIOD; PREOPTIC AREA; REGULATORY MECHANISM; SEX DIFFERENCE; SIGNAL TRANSDUCTION; STRIA TERMINALIS; SUPRACHIASMATIC NUCLEUS; VASOPRESSIN RELEASE; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; SEXUAL DEVELOPMENT;

ANIMALS; BRAIN; ESTRADIOL; FEMALE; GENISTEIN; MALE; MICE; NITRIC OXIDE SYNTHASE TYPE I; PHYTOESTROGENS; SEX CHARACTERISTICS; VASOPRESSINS;

EID: 85011898362     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2017.01.024     Document Type: Article

References (76)

1. Alderton, W.K., Cooper, C.E., Knowles, R.G., Nitric oxide synthases: structure, function and inhibition. Biochem J 357 (2001), 593–615.
2. Allieri, F., Spigolon, G., Melcangi, R.C., Collado, P., Guillamon, A., Gotti, S., Panzica, G.C., Androgen receptor deficiency alters the arginine-vasopressin sexually dimorphic system in TFM rats. Neuroscience 253 (2013), 67–77.
3. Ball, G.F., Balthazart, J., McCarthy, M.M., Is it useful to view the brain as a secondary sexual characteristic?. Neurosci Biobehav Rev 46:Pt 4 (2014), 628–638.
4. Bourguignon, J.P., Slama, R., Bergman, A., Demeneix, B., Ivell, R., Kortenkamp, A., Panzica, G., Trasande, L., Zoeller, R.T., Science-based regulation of endocrine disrupting chemicals in Europe: which approach?. Lancet Diabetes Endocrinol, 2016.
5. Bourque, C.W., Osmoregulation of vasopressin neurons: a synergy of intrinsic and synaptic processes. Prog Brain Res 119 (1999), 59–76.
6. Caldwell, H., Lee, H.-J., Macbeth, A., Young, W., Vasopressin: behavioral roles of an “original” neuropeptide. Prog Neurobiol 84 (2008), 1–24.
7. Campbell, R.E., Herbison, A.E., Gonadal steroid neuromodulation of developing and mature hypothalamic neuronal networks. Curr Opin Neurobiol 29 (2014), 96–102.
8. Cimafranca, M.A., Davila, J., Ekman, G.C., Andrews, R.N., Neese, S.L., Peretz, J., Woodling, K.A., Helferich, W.G., Sarkar, J., Flaws, J.A., Schantz, S.L., Doerge, D.R., Cooke, P.S., Acute and chronic effects of oral genistein administration in neonatal mice. Biol Reprod, 2010.
9. De Vries, G.J., Panzica, G.C., Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138 (2006), 947–955.
10. Dinsdale, E.C., Ward, W.E., Early exposure to soy isoflavones and effects on reproductive health: a review of human and animal studies. Nutrients 2 (2010), 1156–1187.
11. Doerge, D.R., Churchwell, M.I., Chang, H.C., Newbold, R.R., Delclos, K.B., Placental transfer of the soy isoflavone genistein following dietary and gavage administration to Sprague Dawley rats. Reprod Toxicol 15 (2001), 105–110.
12. Doerge, D.R., Twaddle, N.C., Churchwell, M.I., Newbold, R.R., Delclos, K.B., Lactational transfer of the soy isoflavone, genistein, in Sprague-Dawley rats consuming dietary genistein. Reprod Toxicol 21 (2006), 307–312.
13. Forsling, M.L., Kallo, I., Hartley, D.E., Heinze, L., Ladek, R., Coen, C.W., File, S.E., Oestrogen receptor-beta and neurohypophysial hormones: functional interaction and neuroanatomical localisation. Pharmacol Biochem Behav 76 (2003), 535–542.
14. Frye, C., Bo, E., Calamandrei, G., Calza, L., Dessi-Fulgheri, F., Fernandez, M., Fusani, L., Kah, O., Kajta, M., Le Page, Y., Patisaul, H.B., Venerosi, A., Wojtowicz, A.K., Panzica, G.C., Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J Neuroendocrinol 24 (2012), 144–159.
15. Fukushima, A., Furuta, M., Kimura, F., Akema, T., Funabashi, T., Testosterone exposure during the critical period decreases corticotropin-releasing hormone-immunoreactive neurons in the bed nucleus of the stria terminalis of female rats. Neurosci Lett 534 (2013), 64–68.
16. Gore, A.C., Dickerson, S.M., Endocrine disruptors and the developing brain. Colloquium Series in The Developing Brain 3 (2012), 1–114.
17. Gotti, S., Martini, M., Pradotto, M., Viglietti-Panzica, C., Panzica, G.C., Rapid changes on nitrinergic system in female mouse hippocampus during the ovarian cycle. J Chem Neuroanat 38 (2009), 117–123.
18. Gotti, S., Martini, M., Viglietti-Panzica, C., Miceli, D., Panzica, G.C., Effects of estrous cycle and xenoestrogens expositions on mice nitric oxide producing system. Ital J Anat Embryol 115 (2010), 103–108.
19. Gotti, S., Sica, M., Viglietti Panzica, C., Panzica, G.C., Distribution of nitric oxide sythase immunoreactivity in the mouse brain. Microsc Res Tech 68 (2005), 13–35.
20. Grassi, D., Amorim, M.A., Garcia-Segura, L.M., Panzica, G., Estrogen receptor alpha is involved in the estrogenic regulation of arginine vasopressin immunoreactivity in the supraoptic and paraventricular nuclei of ovariectomized rats. Neurosci Lett 474 (2010), 135–139.
21. Grassi, D., Bellini, M.J., Acaz-Fonseca, E., Panzica, G., Garcia-Segura, L.M., Estradiol and testosterone regulate arginine-vasopressin expression in SH-SY5Y human female neuroblastoma cells through estrogen receptors alpha and beta. Endocrinology 154 (2013), 2092–2100.
22. Grassi, D., Lagunas, N., Amorim, M., Pinos, H., Panzica, G., Garcia-Segura, L.M., Collado, P., Role of oestrogen receptors on the modulation of NADPH-diaphorase-positive cell number in supraoptic and paraventricular nuclei of ovariectomised female rats. J Neuroendocrinol 25 (2013), 244–250.
23. Grassi, D., Lagunas, N., Amorin, M., Pinos, H., Panzica, G.C., Garcia-Segura, L.M., Collado, P., Estrogenic regulation of NADPH-diaphorase in the supraoptic and paraventricular nuclei under acute osmotic stress. Neuroscience 248 (2013), 127–135.
24. Grassi, D., Lagunas, N., Pinos, H., Panzica, G., Garcia-Segura, L.M., Collado, P., NADPH-diaphorase colocalizes with GPER and is modulated by the GPER agonist G1 in the SON and PVN of ovariectomized female rats. Neuroendocrinology, 104, 2017 (in press).
25. Guimaraes, R.A., Asth, L., Engelberth, R.C., Cavalcante Jde, S., Soares-Rachetti Vde, P., Gavioli, E.C., Spontaneous failure of the estrous cycle induces anxiogenic-related behaviors in middle-aged female mice. Physiol Behav 147 (2015), 319–323.
26. Hayward, J.N., Pavasuthipaisit, K., Perez-Lopez, F.R., Sofroniew, M.V., Radioimmunoassay of arginine vasopressin in Rhesus monkey plasma. Endocrinology 98 (1976), 975–981.
27. Hull, E.M., Dominguez, J.M., Getting his act together: Roles of glutamate, nitric oxide, and dopamine in the medial preoptic area. Brain Res 1126 (2006), 66–75.
28. Jefferson, W.N., Patisaul, H.B., Williams, C., Reproductive consequences of developmental phytoestrogen exposure. Reproduction 143 (2012), 247–260.
29. Kastenberger, I., Schwarzer, C., GPER1 (GPR30) knockout mice display reduced anxiety and altered stress response in a sex and paradigm dependent manner. Horm Behav 66 (2014), 628–636.
30. Kortenkamp, A., Bourguignon, J.P., Slama, R., Bergman, A., Demeneix, B., Ivell, R., Panzica, G., Trasande, L., Zoeller, R.T., EU regulation of endocrine disruptors: a missed opportunity. Lancet Diabetes Endocrinol., 2016.
31. Lephart, E.D., Setchell, K.D., Handa, R.J., Lund, T.D., Behavioral effects of endocrine-disrupting substances: phytoestrogens. ILAR J 45 (2004), 443–454.
32. Levin, M.C., Sawchenko, P.E., Neuropeptide co-expression in the magnocellular neurosecretory system of the female rat: evidence for differential modulation by estrogen. Neuroscience 54 (1993), 1001–1018.
33. Martini, M., Miceli, D., Gotti, S., Viglietti-Panzica, C., Fissore, E., Palanza, P., Panzica, G.C., Effects of perinatal administration of bisphenol A on the neuronal nitric oxide synthase expressing system in the hypothalamus and limbic system of CD1 mice. J Neuroendocrinol 22 (2010), 1004–1012.
34. Martini, M., Pradotto, M., Panzica, G., Synergic effects of estradiol and progesterone on regulation of the hypothalamic neuronal nitric oxide synthase expression in ovariectomized mice. Brain Res 1404 (2011), 1–9.
35. Mazur, W., Phytoestrogen content in foods. Baillieres Clin Endocrinol Metab 12 (1998), 729–742.
36. McCarthy, M.M., Estradiol and the developing brain. Physiol Rev 88 (2008), 91–134.
37. McCarthy, M.M., Brain sex differences. Brain mapping: an encyclopedic reference Toga, A.W., (eds.) Anatomy and physiology systems, vol. 2, 2015, Elsevier Inc., London (UK), San Diego (USA), 27–35.
38. Nagyeri, G., Valkusz, Z., Radacs, M., Ocsko, T., Hausinger, P., Laszlo, M., Laszlo, F.A., Juhasz, A., Julesz, J., Galfi, M., Behavioral and endocrine effects of chronic exposure to low doses of chlorobenzenes in Wistar rats. Neurotoxicol Teratol 34 (2012), 9–19.
39. Nelson, R.J., Kriegsfeld, L.J., Dawson, V.L., Dawson, T.M., Effects of nitric oxide on neuroendocrine function and behavior. Front Neuroendocrinol 18 (1997), 463–491.
40. Nomura, M., McKenna, E., Korach, K.S., Pfaff, D.W., Ogawa, S., Estrogen receptor-b regulates transcript levels for oxytocin and arginine vasopressin in the hypothalamic paraventricular nucleus of male mice. Mol Brain Res 109 (2002), 84–94.
41. Panzica, G., Melcangi, R.C., Structural and molecular brain sexual differences: a tool to understand sex differences in health and disease. Neurosci Biobehav Rev, 2016.
42. Panzica, G.C., Bo, E., Martini, M.A., Miceli, D., Mura, E., Viglietti-Panzica, C., Gotti, S., Neuropeptides and enzymes are targets for the action of endocrine disrupting chemicals in the vertebrate brain. J Toxicol Environ Health B Crit Rev 14 (2011), 449–472.
43. Panzica, G.C., Mura, E., Miceli, D., Martini, M., Gotti, S., Viglietti Panzica, C., Effects of xenoestrogens on the differentiation of behaviorally-relevant neural circuits in higher vertebrates. Vaudry, H., et al. (eds.) Trends in comparative endocrinology and neurobiology, vol. 1163, 2009, New York Academy of Sciences, New York, NY, 271–278.
44. Panzica, G.C., Viglietti-Panzica, C., Mura, E., Quinn, M.J. Jr, Palanza, P., Ottinger, M.A., Effects of xenoestrogens on the differentiation of behaviorally relevant neural circuits. Front Neuroendocrinol 28 (2007), 179–200.
45. Panzica, G.C., Viglietti-Panzica, C., Sica, M., Gotti, S., Martini, M., Pinos, H., Carrillo, B., Collado, P., Effects of gonadal hormones on central nitric oxide producing systems. Neuroscience 138 (2006), 987–995.
46. Paxinos, G., Franklin, K.B.J., The mouse brain in stereotaxic coordinates. 2001, Academi Press, San Diego.
47. Pierman, S., Sica, M., Allieri, F., Viglietti-Panzica, C., Panzica, G.C., Bakker, J., Activational effects of estradiol and dihydrotestosterone on social recognition and the arginine-vasopressin immunoreactive system in male mice lacking a functional aromatase gene. Horm Behav 54 (2008), 98–106.
48. Piet, R., Fraissenon, A., Boehm, U., Herbison, A.E., Estrogen permits vasopressin signaling in preoptic kisspeptin neurons in the female mouse. J Neurosci 35 (2015), 6881–6892.
49. Prast, H., Philippu, A., Nitric oxide as modulator of neuronal function. Prog Neurobiol 64 (2001), 51–68.
50. Rebuli, M.E., Patisaul, H.B., Assessment of sex specific endocrine disrupting effects in the prenatal and pre-pubertal rodent brain. J Steroid Biochem Mol Biol 160 (2016), 148–159.
51. Richter, C.A., Birnbaum, L.S., Farabollini, F., Newbold, R.R., Rubin, B.S., Talsness, C.E., Vandenbergh, J.G., Walser-Kuntz, D.R., vom Saal, F.S., In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 24 (2007), 199–224.
52. Rodrigo, J., Springall, D.R., Uttenthal, O., Bentura, M.L., Abadia-Molina, F., Riveros-Moreno, V., Martinez-Murillo, R., Polak, J.M., Moncada, S., Localization of nitric oxide synthase in the adult rat brain. Philos Trans R Soc Lond B Biol Sci 345 (1994), 175–221.
53. Rodriguez-Gomez, A., Filice, F., Gotti, S., Panzica, G., Perinatal exposure to genistein affects the normal development of anxiety and aggressive behaviors and nitric oxide system in CD1 male mice. Physiol Behav 133 (2014), 107–114.
54. Rood, B.D., De Vries, G.J., Vasopressin innervation of the mouse (Mus musculus) brain and spinal cord. J Comp Neurol 519 (2011), 2434–2474.
55. Rood, B.D., Stott, R.T., You, S., Smith, C.J., Woodbury, M.E., De Vries, G.J., Site of origin of and sex differences in the vasopressin innervation of the mouse (Mus musculus) brain. J Comp Neurol 521 (2013), 2321–2358.
56. Roque, S., Mesquita, A.R., Palha, J.A., Sousa, N., Correia-Neves, M., The behavioral and immunological impact of maternal separation: a matter of timing. Front Behav Neurosci, 8, 2014, 192.
57. Routledge, E.J., White, R., Parker, M.G., Sumpter, J.P., Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J Biol Chem 275 (2000), 35986–35993.
58. Royston, S.E., Bunick, D., Mahoney, M.M., Oestradiol exposure early in life programs daily and circadian activity rhythms in adult mice. J Neuroendocrinol, 28, 2016, 10.1111/jne.12335.
59. Rozman, K.K., Bhatia, J., Calafat, A.M., Chambers, C., Culty, M., Etzel, R.A., Flaws, J.A., Hansen, D.K., Hoyer, P.B., Jeffery, E.H., Kesner, J.S., Marty, S., Thomas, J.A., Umbach, D., NTP-CERHR expert panel report on the reproductive and developmental toxicity of soy formula. Birth Defects Res B Dev Reprod Toxicol 77 (2006), 280–397.
60. Scallet, A.C., Wofford, M., Meredith, J.C., Allaben, W.T., Ferguson, S.A., Dietary exposure to genistein increases vasopressin but does not alter beta-endorphin in the rat hypothalamus. Toxicol Sci 72 (2003), 296–300.
61. Scordalakes, E.M., Rissman, E.F., Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estrogen receptor alpha. Genes Brain and Behav 3 (2004), 20–26.
62. Scordalakes, E.M., Shetty, S.J., Rissman, E.F., Roles of estrogen receptor alpha and androgen receptor in the regulation of neuronal nitric oxide synthase. J Comp Neurol 453 (2002), 336–344.
63. Sica, M., Martini, M., Viglietti-Panzica, C., Panzica, G.C., Estrous cycle influences the expression of neuronal nitric oxide synthase in the hypothalamus and limbic system of female mice. BMC Neurosci, 10, 2009 78 (01–14).
64. Skowsky, W.R., Swan, L., Smith, P., Effects of sex steroid hormones on arginine vasopressin in intact and castrated male and female rats. Endocrinology 104 (1979), 105–108.
65. Slama, R., Bourguignon, J.P., Demeneix, B., Ivell, R., Panzica, G., Kortenkamp, A., Zoeller, T., Scientific issues relevant to setting regulatory criteria to identify endocrine disrupting substances in the European Union. Environ Health Perspect 124 (2016), 1497–1503.
66. Sofroniew, M.V., Madler, M., Muller, O.A., Scriba, P.C., A method for the consistent production of high quality antisera to small peptide hormones. Fresenius Z Anal Chem 290 (1978), 163–164.
67. Sofroniew, M.V., Weindl, A., Schinko, I., Wetzstein, R., The distribution of vasopressin- oxytocin and neurophysin-producing neurons in the guinea pig brain. I. The classical hypothalamo-neurohypyseal system. Cell Tissue Res 196 (1979), 367–384.
68. Sullivan, A.W., Beach, E.C., La, Stetzik., Perry, A., D'Addezio, A.S., Cushing, B.S., Patisaul, H.B., A novel model for neuroendocrine toxicology: neurobehavioral effects of BPA exposure in a prosocial species, the prairie vole (Microtus ochrogaster). Endocrinology 155 (2014), 3867–3881.
69. Swaab, D.F., Ageing of the human hypothalamus. Horm Res 43 (1995), 8–11.
70. Vega, C., Moreno-Carranza, B., Zamorano, M., Quintanar-Stephano, A., Mendez, I., Thebault, S., Martinez de la Escalera, G., Clapp, C., Prolactin promotes oxytocin and vasopressin release by activating neuronal nitric oxide synthase in the supraoptic and paraventricular nuclei. Am J Physiol Regul Integr Comp Physiol 299 (2010), R1701–R1708.
71. Viglietti-Panzica, C., Mura, E., Panzica, G.C., Effects of early embryonic exposure to genistein on male copulatory behavior and vasotocin system of Japanese quail. Horm Behav 51 (2007), 355–363.
72. Wang, L., Andersson, S., Warner, M., Gustafsson, J.A., Estrogen actions in the brain. Science Signaling, 138, 2002, pe29, 10.1126/stke.2002.138.pe29.
73. Watson, R.E., Wiegand, S.J., Clough, R.W., Hoffman, G.E., Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7 (1986), 155–159.
74. Wisniewski, A.B., Cernetich, A., Gearhart, J.P., Klein, S.L., Perinatal exposure to genistein alters reproductive development and aggressive behavior in male mice. Physiol Behav 84 (2005), 327–334.
75. Young, K.A., Gobrogge, K.L., Liu, Y., Wang, Z., The neurobiology of pair bonding: insights from a socially monogamous rodent. Front Neuroendocrinol 32 (2011), 53–69.
76. Zhang, L., Tong, M., Xiao, M., Li, L., Ding, J., Nitric oxide mediates feedback inhibition in angiotensin II-induced upregulation of vasopressin mRNA. Peptides 30 (2009), 913–917.